Weakened purifying selection leads to elevated mutation load under environmental sex determination

Abstract

In many gonochoristic taxa, sex is influenced by developmental environment, a system that can lead to temporal fluctuations in offspring sex ratio. Demographic models suggest that only short-lived species with environmental sex determination (ESD) are negatively impacted by sex-ratio fluctuations, yet these models fail to account for the potential mutation load associated with reductions in genetically effective population sizes. In this study, we developed a series of individual-based simulation models that explore the fixation rates of mildly deleterious alleles under different sex-determining systems and examine the impacts of variation in lifespan and offspring sex ratio. Populations with ESD exhibited increases in fixation rates in both short- and long-lived populations, but substantial increases were limited to populations characterized by a combination of high sex-ratio variation and short lifespan. Fixation rates were negatively associated with effective population size, indicating that purifying selection operates less efficiently under ESD relative to genotypic sex determination. Reductions in effective population size could be attributed to both intragenerational forces (unequal sex ratio) and intergenerational forces (variable census population sizes). Levels of temporal sex-ratio variation calculated from wild populations of ESD species were capable of yielding large increases in fixation rates, although this relationship was strongly mediated by lifespan. Our results may help to explain the limited phylogenetic distribution of ESD in short-lived taxa.